Down to the bone: the role of overlooked endolithic microbiomes in reef coral health

Abstract

Reef-building corals harbour an astonishing diversity of microorganisms, including endosymbiotic microalgae, bacteria, archaea, and fungi. The metabolic interactions within this symbiotic consortium are fundamental to the ecological success of corals and the unique productivity of coral reef ecosystems. Over the last two decades, scientific efforts have been primarily channelled into dissecting the symbioses occurring in coral tissues. Although easily accessible, this compartment is only 2-3 mm thick, whereas the underlying calcium carbonate skeleton occupies the vast internal volume of corals. Far from being devoid of life, the skeleton harbours a wide array of algae, endolithic fungi, heterotrophic bacteria, and other boring eukaryotes, often forming distinct bands visible to the bare eye. Some of the critical functions of these endolithic microorganisms in coral health, such as nutrient cycling and metabolite transfer, which could enable the survival of corals during thermal stress, have long been demonstrated. In addition, some of these microorganisms can dissolve calcium carbonate, weakening the coral skeleton and therefore may play a major role in reef erosion. Yet, experimental data are wanting due to methodological limitations. Recent technological and conceptual advances now allow us to tease apart the complex physical, ecological, and chemical interactions at the heart of coral endolithic microbial communities. These new capabilities have resulted in an excellent body of research and provide an exciting outlook to further address the functional microbial ecology of the "overlooked" coral skeleton.

Fig. 1

Spatial structure and physicochemical environment experienced by microbes within the coral skeleton. The close-up depicts a typical skeletal pore populated by a range of autotrophic (green) and heterotrophic microbes (other colours). These organisms typically experience daily fluctuations in pH (from 7.5–8.5) [41], oxygen (10–210% air saturation) [15] and light (0–10% of PAR and 0–80% of NIR) [29]. In addition, they are exposed to enriched levels of dissolved inorganic phosphorus (DIP) and to concentrations of dissolved inorganic nitrogen (DIN) 10 times higher than in reef water [31, 40]. Outline of the coral from [54]

Fig. 2

Climate change affects endolithic microbiomes and their interactions with the coral host. a In the intact symbiosis, the nutrient exchange between coral cells and the endosymbiotic microalgae is maintained. In this scenario, endoliths remain deep in the skeleton. b Exposure to prolonged high-temperature anomalies causes the loss of Symbiodiniaceae from coral tissues, resulting in bleaching. Subsequently more light penetrates into the skeleton, causing endolithic microbiomes to bloom. Endoliths were previously shown to increase their biomass and primary production, physically reaching the animal tissues, and enhance the rates of organic carbon (photoassimilate) translocation to the animal host. It is hypothesized that nutrient exchange between the coral host and endoliths may potentially help the coral animal to survive or even to recover from bleaching. At the same time, the increased growth of endoliths may cause microbioerosion to intensify, undermining the structural integrity of the coral skeleton, and rendering the coral colony more vulnerable to breakage (e.g., during storm events)

Fig. 3

Proposed workflow to untangle the metabolic interactions occurring between microbes in the coral skeleton and between skeleton and tissue communities. Methods used at each step are outlined in grey